Download Feather-picking Psittacines: Histopathology and

Survey
yes no Was this document useful for you?
   Thank you for your participation!

* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project

Document related concepts
no text concepts found
Transcript
Vet Pathol 45:401–408 (2008)
Feather-picking Psittacines: Histopathology and Species Trends
M. M. GARNER, S. L. CLUBB, M. A. MITCHELL,
AND
L. BROWN
Northwest ZooPath, Monroe, WA (MMG); The Rainforest Clinic for Birds & Exotics, Loxahatchee,
FL (SLC); Louisiana State University, Department of Veterinary Clinical Sciences, School of Veterinary
Medicine, Baton Rouge, LA (MAM); Histology Consulting Service, Everson, WA (LB)
Abstract. Histologic findings are described for 408 feather-picking or self-mutilating psittacines with
the use of biopsies from clinically affected and unaffected skin. Inflammatory skin disease was diagnosed
in 210 birds, and traumatic skin disease was diagnosed in 198 birds. Criteria used for the diagnosis of
inflammatory skin disease included the presence of perivascular inflammation in the superficial or deep
dermis of clinically affected and unaffected sites. The primary histologic criteria for the diagnosis of
traumatic skin disease were superficial dermal scarring with or without inflammation in the affected sites
and an absence of inflammation in the unaffected sites. The inflammatory cells associated with the
lesions were typically lymphocytes and occasionally plasma cells, histiocytes, and granulocytes. A
preponderance of inflammatory skin disease was seen in macaws (Ara spp.) and Amazon parrots
(Amazona spp.). A preponderance of traumatic skin disease was seen in cockatoos (Cacatua spp.) and
African grey parrots (Psittacus erithacus). The prevalence of each was approximately equal in several
other species, including conures (Aratinga and Pyrrhura spp.), eclectus parrots (Eclectus roratus), quaker
parrots (Myiopsitta monachus), cockatiels (Nymphicus hollandicus), parakeets (Cyanorhamphus and
Psittacula spp.), and caiques (Pionites spp.). No geographic or gender-based trends were identified.
These findings could be helpful for identifying and treating birds with feather-picking disorders.
Key words:
Dermatitis; feather picking; histopathology; parrot; psittacine; self-mutilation.
Diseases of the skin constitute a large proportion
of case submissions to veterinary diagnostic laboratories, and many distinct entities have been well
characterized, especially in domestic mammals.
Patterns of histologic change reliably identify
specific entities and pathogenic events, such as
hypersensitivity dermatitis, vasculitis, and autoimmune skin disease.4 Pattern-based histologic interpretation of skin disease is not documented in
birds, although extrapolation from the mammalian
literature might be applicable to some avian
cutaneous lesions, such as follicular dysplasia,
vasculitis, and hypersensitivity.3 Intradermal allergy testing has been attempted in psittacines but
with ambiguous results.7 As with mammalian
skin disorders, skin biopsy appears to provide
useful diagnostic information for avian skin
disorders.1–3,11,12
Feather loss or destructive behavior and selfmutilation of the skin are common problems in
captive birds, particularly psittacines.1–3,11,12 A
number of causes have been identified or suggested,
including mycotic, bacterial, viral, and parasitic
agents; hypersensitivity; hormonal derangements;
hepatic or pancreatic disease; and psychogenic
disorders.1–3,5,8,10–12 Pathologists working with skin
biopsies from feather-picking birds have recognized
histologic patterns in affected skin that suggest an
inflammatory basis for this behavior in some birds,
whereas other birds have lesions attributed only to
self-induced trauma.1–3,11 Remarkably, at least 1
report suggests that inflammation is not a contributing factor for feather picking in psittacines.10 Our
study summarizes histologic findings of a retrospective study of paired biopsies from birds with
feather loss, feather picking, or self-mutilating
behavior and determines the presence or absence
of inflammation not attributed to trauma in these
birds.
Materials and Methods
Animals
A retrospective study of avian skin disease was
conducted from cases submitted to Northwest ZooPath
during the years 1994–2005. All cases diagnosed or
coded with dermatitis, skin trauma, inflammatory skin
disease, psychogenic disorder, self-mutilation, or feather
picking were reviewed. From this group, all cases that
had sample collection compliant with a paired biopsy
protocol1 received further consideration, whereas remaining cases were excluded from the study. Any cases
that had histologically recognizable infectious agents,
neoplasia, or follicular dysplasia also were excluded
from this study.
401
402
Garner, Clubb, Mitchell, and Brown
Vet Pathol 45:3, 2008
Fig. 2. Skin; African grey parrot. Note feather
tracts with emerging blood feathers (arrow), and empty
follicular ostia where feathers have been pulled by the
bird but new blood feathers have not yet emerged
(arrowhead). Wedge biopsies should include feather
follicles that contain blood feathers and surrounding
skin.
Fig. 1. Inflammatory skin disease; scarlet macaw
(Ara macao). Note loss of contour feathers over the
chest, ventral aspects of the neck, left leg, and over the
patagium. These areas are easily reached by the beak
and feet.
Biopsy technique
Biopsies were obtained from affected and unaffected
sites of birds that had evidence of feather picking,
feather loss, or dermatitis (Fig. 1). The paired biopsy
protocol requested that clearly labeled full-thickness
wedge biopsies of skin and feather be obtained from
affected and unaffected sites on the same bird and fixed
routinely in formalin for histologic examination. Sites
were to include a blood feather and or feather tract if
possible (Fig. 2). Affected sites were clinically abnormal
and usually were areas easily reached by the bird’s beak
such as the legs or chest. Unaffected sites were areas that
appeared clinically normal or were not easily reached by
the bird, such as the top of the head or back of the neck.
Good sectioning of feathered skin requires much
practice, and the technique is described in detail herein:
Normal and abnormal samples were processed identi-
cally, except that the normal samples were inked black
(Cancer Diagnostics, Inc. Catalog No. 0728-1, Cancer
Diagnostics, Inc., PO Box 1205 Birmingham, MI 48021)
with a cotton tip swab and allowed to dry for 3 minutes
before proceeding with trimming. The samples underwent routine overnight processing and were embedded
in type 9 paraffin (Catalog No. 8337, Richard Allan
Scientific, 225 Parsons Street, Kalamazoo, MI 49007).
After cooling the paraffin sample block and facing into
the block, the sample was returned to the wet ice tray for
5–10 minutes. An initial section was then cut at 4 mm
and laid out onto a 43uC distilled water tissue float bath.
Then after again facing into the block approximately
60–100 mm, depending on the size of the feather sample,
the sample block was allowed to soften on a wet ice tray
for 5–10 minutes before sectioning. This process was
repeated for a total of 3 levels. The slides were placed
into a slide dryer oven at 75uC. for 30 minutes. The
slides were then stained routinely with hematoxylin and
eosin (HE).
Histologic criteria
A histologic section of normal skin and follicle with
blood feather is illustrated in Fig. 3. The primary
histologic criteria for the diagnosis of traumatic skin
disease were superficial dermal scarring in the affected
sites (Fig. 4) and a general absence of inflammation in
the unaffected sites. Additional lesions attributed to
beak or foot trauma included feather crush, stripping of
the shaft and barbules (Fig. 5), and retroflexion of the
barbules because of adhesions to the inner follicular
sheath at the level of the infundibulum (Figs. 6, 7).
Affected sites sometimes also had varying degrees of
Vet Pathol 45:3, 2008
Feather-picking Parrots
Fig. 3. Normal skin and blood feather; Blue and
gold macaw (Ara ararauna). Note inner (i) and outer (o)
follicular sheaths, pulp cavity (p), infundibulum (arrows), and emerging barbules (arrowhead). Inset:
Higher magnification of skin adjacent to a follicle,
showing 1–2-cell thickness of normal epidermis, dermal
collagen fibers, and a small blood vessel in the
superficial dermis (arrow). HE.
Fig. 4. Traumatic dermatitis; Mollucan cockatoo
(Cacatua moluccensis). Note increased thickness of epidermis and mild compact hyperkeratosis (compared with
Fig. 3), foci of superficial dermal scarring (arrows), and
foci of perivascular inflammation. HE. Bar 5 200 mm.
403
Fig. 5. Feather trauma; African grey parrot. Note
frayed (arrows) and scalloped (arrowheads) foci on the
external surface of the inner follicular sheath from beak
trauma incurred while pulling on the shaft. Compare
with the external surface of the normal feather sheath in
Fig. 7. HE.
epidermal hyperplasia, compact orthokeratotic hyperkeratosis, and perivascular to diffuse inflammation.
Inflammation was typically characterized by the presence of lymphocytes, plasma cells, and histiocytes,
although eosinophilic granulocytes (heterophils or
eosinophils) were occasionally seen, particularly in
ulcerated skin lesions. These birds sometimes also had
some scarring in the unaffected sites. Rarely, perivascular inflammation was also seen in unaffected sites but
was considered disproportionately mild compared with
the extent and severity of the dermal scarring.
Criteria used for the diagnosis of inflammatory skin
disease included the presence of mild to marked
perivascular inflammation in the superficial or deep
dermis of clinically affected and unaffected sites (Fig. 8).
The inflammatory cells typically associated with the
lesions were lymphocytes with fewer plasma cells,
histiocytes, and eosinophilic granulocytes. Varying
degrees of edema, epidermal and follicular hyperkeratosis, and perivascular pulpitis were also present in some
cases. For most cases, it was necessary to examine all 3
404
Garner, Clubb, Mitchell, and Brown
Fig. 6. Traumatic dermatitis; cockatoo. An indentation of the inner sheath (arrowhead) and disorganized
barbules across the width of the feather (arrows)
correspond to a focus of beak crush where the feather
emerges from the follicle. The large clear spaces within
the feather are artifacts of sectioning. HE.
levels of the biopsies to confirm the presence of
inflammation, especially in unaffected sites. Cases with
histologic evidence of trauma in the unaffected site
generally were not included in the inflammatory skin
disease group, to avoid confusion regarding the
pathogenesis of the inflammation; however, few cases
were included in this subset if the scarring was
disproportionately mild compared with the severity of
the inflammatory process.
Statistical analysis
The 95% binomial confidence intervals (CI) were
calculated for each of the proportion estimates. For
cases in which the prevalence estimate was 0, the 95%
confidence intervals were estimated as previously
described.13 The chi-square test for homogeneity was
used to determine whether species, gender, or submission date had an effect on the histopathologic findings.
Logistic regression analysis was then used to evaluate
the effect of the different independent variables (species,
gender, or submission date [time]) simultaneously on
outcome (traumatic or inflammatory skin disease). Age
could not be included in the model because it was not
available. Main effects variables were removed individually from full models to assess the effects on the model
Vet Pathol 45:3, 2008
Fig. 7. Higher magnification of feather in Fig. 6;
cockatoo. Note retroflexion of the emerging barbules (b)
associated with apparent adhesions to the inner surface
of the inner sheath (arrows), and attributed to beakinduced feather crush. Adjacent barbules are not
affected (arrowheads). The outer surface of the external
sheath is normal. HE.
likelihood ratio statistics, magnitude of the coefficients
for other variables, and Hosmer Lemeshow goodness of
fit statistics. Interactions between the main effects
variables were also evaluated in the models. SPSS 11.0
(SPSS Inc., Chicago, IL) was used for the analysis. A P
, .05 was considered statistically significant.
Results
From 1994 to 2005, 16,162 avian biopsies or
necropsies were accessioned at Northwest ZooPath. Dermatitis or skin trauma was diagnosed in
1,183 birds (7.3%, 95% confidence interval [CI] 5.8–
8.7). With the use of paired biopsy criteria, 408
psittacines were included in the study.
The prevalence of inflammatory skin disease in
the sample population was 51.5% (210/408; 95% CI
46.2–55.8), whereas the prevalence of traumatic
skin disease was 48.5% (198/408; 95% CI 44.2–
53.8). Differences in the type of diagnosis (trau-
405
Feather-picking Parrots
Vet Pathol 45:3, 2008
and amazons were significantly more likely to have
inflammatory skin disease (Table 1). Statistically
significant differences were not seen for conures
(Aratinga and Pyrrhura spp.), eclectus parrots
(Eclectus roratus), quaker parrots (Myiopsitta
monachus), cockatiels (Nymphicus hollandicus),
parakeets (Cyanorhamphus and Psittacula spp.),
caiques (Pionites spp.), lovebirds (Agapornis spp.),
or parrotlets; for hawk-headed (Deroptyus accipitrinus), Senegal (Poicephalus senegalus), Jardine
(Poicephalus gulielmi), or Alexandrine (Psittacula
eupatria) parrots; or for parrots of unknown genus.
In this study, 115 (28.2%) birds were male, 131
(32.1%) were female, and 162 were of unknown
gender (39.7%). There was a significant difference
in the diagnoses between female and unknown
gender (x2 8.7, P 5 .01) (Table 2). On the basis of
the 95% CI, there was also a significant difference
in the diagnoses within unknown gender (Table 2).
Skin biopsy samples were received every month
and averaged from 5.1% (August) to 15.3% (July).
Sample submission was skewed for the month of
February (15.3%), however, as a result of a large
number of lorikeet samples being submitted from
the same collection. There did not appear to be any
difference in distribution of inflammatory or traumatic skin disease on the basis of location of the bird
within the United States at the time of biopsy.
In the final logistic regression model, only species
(x2 13.9, P 5 .0001) was included in the model.
Fig. 8. Inflammatory skin disease; Eclectus parrot
(Eclectus roratus). Note moderate perivascular inflammatory cell cuff in the superficial dermis, lack of
scarring, and normal epidermal thickness. This biopsy
was from a clinically unaffected site on the back of the
head. HE. Bar 5 100 mm.
matic or inflammatory) made for cockatoos
(Cacatua spp.), African grey parrots (Psittacus
erithacus), macaws (Ara spp.), lorikeets and lories
(Subfamily Loriinae), and Amazon parrots (Amazona spp.) were significant on the basis of the 95%
CI (Table 1). Cockatoos and African grey parrots
were significantly more likely to have traumainduced skin disease, whereas macaws, lorikeets,
Table 1. Prevalence and 95% CI of traumatic and inflammatory skin lesions observed in psittacines from
Northwest ZooPath.
Traumatic
Inflammatory
Group
n
Percent
95% CI
Percent
95% CI
Cockatoo
African grey
Macaw
Lorikeets
Amazon
Conure
Eclectus
Quaker
Lovebird
Cockatiel
Parakeet
Caique
Hawkshead
‘‘Parrot’’
Senegal
Jardine
Alexandrine
Parrotlet
98
77
48
39
30
28
22
13
11
11
7
6
4
4
3
3
2
2
73.5*
74.0*
20.8*
0.0*
23.3*
46.4
36.4
46.2
54.5
54.5
57.2
33.3
25.0
50.0
33.3
33.3
0.0
50
64.7–82.2
64.0–84.0
9.3–32.3
0–7.6**
8.2–38.4
27.9–64.8
16.4–56.4
19.1–73.3
25.1–83.9
25.1–83.9
20.5–93.8
4.4–71.0
0.0–67.4
1.0–99.0
0.0–86.6
0.0–86.6
26.5*
26.0*
79.2*
100.0*
76.7*
53.6
63.6
53.8
45.5
45.5
42.8
66.7
75.0
50.0
66.7
66.7
100
50
17.7–35.2
16.0–36.0
67.7–90.7
* Significant difference between diagnoses.
61.6–91.8
35.1–72.1
43.6–83.6
26.7–80.9
16.1–74.9
16.1–74.9
6.1–79.4
29.7–100
32.6–100.0
1.0–99.0
13.4–100.0
13.4–100.0
406
Garner, Clubb, Mitchell, and Brown
Table 2.
Vet Pathol 45:3, 2008
Prevalence of skin lesions by gender.
Traumatic
Inflammatory
Gender
n
Percent
95% CI
Percent
95% CI
Male
Female
Unknown
115
131
162
47.8
58.0**
40.7* **
38.7–56.9
49.5–66.4
33.1–48.2
52.2
42.0
59.3*
43.1–61.3
33.5–50.4
51.7–66.8
* Significant difference between diagnoses according to 95% CI.
** Significant difference between gender (P 5 .01).
There were no significant interaction terms. The
final model was: traumatic feather disease 5 20.36
+ 0.090 3 species.
Discussion
A ‘‘paired’’ biopsy protocol was devised to aid in
understanding the cause or causes of feather
picking or self-mutilation in birds,1 and this study
summarizes data collected with this protocol.
Psittacines have ample beaks and claws and are
adroit at scratching or chewing most parts of the
body, for whatever reason. The top of the head and
back of the neck often are the areas that are spared
in birds presenting with advanced alopecia or
evidence of self-mutilation.3 Therefore, these areas
seem most likely to have the least histologic change
attributed to excoriation and were the preferred
sites for specimens designated as ‘‘unaffected’’;
also, it seemed logical that parrots with generalized
inflammatory skin disease would have inflammatory changes in the sites with less or no excoriative
change. The results of this study supported these
suppositions, and histologic findings in the unaffected sites were essential for designations of
inflammatory or noninflammatory skin disease.
In most of the authors’ cases it is felt that biopsy of
a traumatized site alone would not provide
sufficient information for determining the presence
of an underlying inflammatory process, because
inflammation would be a component of the tissue
response to beak or foot trauma.
The cause for traumatic skin disease in these
birds was not determined; a number of causes have
been proposed, including behavioral problems,
hormonal imbalances, infectious agents, follicular
dysplasia, and hypersensitivity.1–3,11,12 The results of
this study indicate that a subgroup of traumatic
skin disease likely exists that is not associated with
underlying inflammatory skin disease, infectious
agents or follicular dysplasia. For these birds, a
psychogenic abnormality is considered possible,
but this could be difficult to prove. Particularly
interesting are the trends identified in the study for
certain species. A large proportion of the cockatoos
and African grey parrots had traumatic skin
disease, 2 groups of parrots that are notorious for
feather-picking behavior in captivity;1–3 however, a
smaller number of cockatoos and grey parrots also
had inflammatory skin disease on the basis of study
criteria, so biopsy is considered important to fully
characterize the lesions associated with feather
picking in these species.
Our findings support previous reports that
inflammatory skin disease might be prevalent in
feather-picking birds on the basis of examination of
paired biopsy specimens.1,2 Inflammatory skin
disease was seen in all parrot species in the study
and was the predominant presentation in macaws
and Amazon parrots. The etiology for inflammatory skin disease in the study birds was not
determined. The pattern and the cellular constituents of the inflammation are most suggestive of
cutaneous delayed type hypersensitivity.4,9
Hypersensitivity is a type of inflammatory
reaction caused by an excessive immunologic
response. In birds, acute and delayed type hypersensitivity reactions can be elicited to a variety of
antigens, including histamine, ConA, pokeweed
mitogen, and bovine albumin. In birds, delayedtype hypersensitivity is caused by cell-mediated
immune responses occurring at least 24 hours after
antigen contact with sensitized T cells. The
inflammatory reaction in the skin of birds with
delayed type hypersensitivity appears to be similar
to that of mammals and comprises primarily
perivascular sensitized T cells, although histiocytes,
heterophils, and eosinophils can also be components of the inflammatory reaction.9 The pattern
and cellular constituents of the inflammatory
response in the birds of this study were similar to
those described for experimentally induced hypersensitivity, especially in those birds that lacked a
significant traumatic component to the lesion. In
this regard, it is considered probable that the
inflammatory reactions seen in the ‘‘unaffected’’
sites could be due, at least in part, to some form of
hypersensitivity. These reactions might have been a
source of discomfort or pruritus for the birds and
Vet Pathol 45:3, 2008
407
Feather-picking Parrots
thus could have been a cause of the feather picking
or self-mutilation.
Sectioning feathers for optimal histologic examination can be difficult. Our technique, described in
detail herein, was refined over several years. It was
necessary to examine at least 3 sections in the block
for many of the cases, especially in the ‘‘unaffected’’ sites, to detect inflammatory changes, indicating that a thorough microscopic examination is
necessary to document the inflammation in some
cases. In a detailed report of the normal histology
of the avian integument, inflammation is not
described.6 Inflammation for which the cause
cannot be identified probably should not be
regarded as nonspecific, incidental, or insignificant.
In the authors’ opinion, the presence of inflammation in the skin of birds is not normal, can be a
source of discomfort or pruritus for affected birds,
and provides at least one plausible explanation for
the feather picking or self-mutilation seen in some
psittacines. On the basis of the large number of
affected species, obvious species trends, and wide
demographic distribution of affected birds, it is
considered likely that more than 1 etiologic event
might exist. Our findings are in contrast to those of
a previously published report that did not associate
inflammatory skin disease with feather-picking
birds.10 Although that study had a similar species
distribution, sample size was much smaller (8 birds
total), and a paired sampling technique with
multilevel histologic examination was not used.
Future studies similar to those in chickens9
documenting the phenotype of inflammatory cells
in the skin lesions with immunohistochemistry
might prove useful in further differentiating these
inflammatory and traumatic lesions.
The outcome between females and birds of
unknown gender, and between birds of unknown
gender was significantly different. This might not
be unexpected in that the number of birds of
unknown gender was greater than the number of
female birds, and it is difficult to ascertain the
gender of psittacines without molecular or surgical
testing. The fact that there was no difference
between known males and females, suggests that
a difference between females and unknown genders
might disappear if the genders were known. The
difference between known genders is likely the
result of an overrepresentation of those species
found with inflammatory disease (e.g., macaws,
lorikeets, and amazons) that had never been sexed.
No seasonal trends were noted for traumatic or
inflammatory skin disease; however, these data
should be interpreted conservatively regarding
seasonal occurrence. Many of the birds had a long
history of feather-picking or self-mutilating behavior and the precise onset of the condition might not
have been known, or the biopsies might not have
been obtained at the precise onset of the condition.
All of the lorikeets in the study had inflammatory skin disease; however, all were from a single
captive population. Lorikeets and lories are common pet and exhibit species and are widely
distributed in captivity. The study findings suggest
that lorikeets could be susceptible to inflammatory
skin disease, but that it might not be common in
the general captive population. No budgerigars
(Melopsittacus undulatus) met the criteria for this
study, suggesting that this common pet species
might not be prone to feather-picking behavior or
self-mutilation. Very few nonpsittacine cases fit
criteria for inclusion in this study (data not shown),
perhaps because fewer dermatopathies are recognized because of less human contact with these
birds or because a lower prevalence of inflammatory skin disease exists for nonpsittacine species.
Our findings indicate that inflammatory skin
disease and traumatic skin disease occur in featherpicking or self-mutilating birds and appear to be
distinct entities and that species trends exist for
both presentations. Paired samples from clinically
affected and unaffected sites are helpful aids for the
pathologist interpreting biopsies from these patients. We emphasize the importance of examining
sections at multiple levels in the block to lessen the
possibility that inflammatory changes are overlooked.
Acknowledgements
Northwest ZooPath is grateful to the following
institutions for submission of study cases: Avicultural
Breeding & Research, Loxahatchee, FL; All Creatures
Vet Hospital, Stuart, FL; All Creatures Animal Hospital, Bremerton, WA; Angell Animal Medical Center,
Boston, MA; Animal Hospital of Centereach, Centereach, NY; Animal Health Clinic, Jupiter, FL; Barberton
Vet Clinic, Norton, OH; Bethel Park Animal Hospital,
Bethel Park, PA; Bird & Exotic Clinic of Seattle, Seattle,
WA; Dallas Zoo, Dallas, TX; Des Moines Vet Hospital,
Des Moines, WA; Djurkliniken Roslagstull, Stockholm,
Sweden; Ellensburg Animal Hospital, Ellensburg, WA;
Floridawild Vet Hospital, Deland, FL; Fort Worth Zoo,
Fort Worth, TX; Guardian Animal Hospital, Ashland,
KY; Hendricks County Animal Hospital, Danville, IN;
Dr. Jackie Gai, Vacaville, CA; Kansas State University,
Manhattan, KS; Karlskrona Distr. Vet Station, Lyckeby, Sweden; Kraft Mobile Vet Services, Snohomish,
WA; Los Angeles Zoo, Los Angeles, CA; Latah Creek
Animal Hospital, Camano Island, WA; Old County
Animal Clinic, Plainview, NY; Dr. Susan Clubb,
Loxahatchee, FL; Regiondjursjukhuset Helsingborg,
Helsingborg, Sweden; Safari Animal Care Center,
408
Garner, Clubb, Mitchell, and Brown
League City, TX; Sno-Wood Vet Hospital, Snohomish,
WA; Summertree Animal & Bird Clinic, Dallas, TX;
The Toledo Zoo, Toledo, OH; Valley Animal Hospital,
Roanoke, VA; Village Vet Hospital, Bellingham, WA;
West Valley Pet Clinic, Woodland Hills, CA; Windcrest
Animal Hospital, Wilmington, DE; and Yukon Vet
Hospital, Yukon, OK. The authors also thank Jamie
Kinion for data retrieval and Christie Buie for photo
editing, illustration layout, and manuscript submission.
References
1 Clubb SL, Garner MM, Cray C: Detection of
inflammatory skin disease in psittacine birds using
paired skin biopsies, Proc Assoc Avian Vet, Monterey, CA, pp. 193–199, 2002.
2 Clubb SL, Garner MM, Cray C, Arheart K,
Goodman M: Diagnostic assessment of feather
damaging behavior in African grey parrots (Psittacus erithacus), Proc Assoc Avian Vet, New Orleans,
LA, pp. 313–320, 2004.
3 Garner MM: Avian noninfectious skin disorders,
Proc Assoc Avian Vet, Pittsburgh, PA, pp. 21–23,
2003.
4 Gross TL, Ihrke PJ, Walder EJ, Affolter VK:
Diseases of the dermis. In: Skin Diseases of the
Dog and Cat, Clinical and Histopathological Diagnosis, ed. Gross TL, Ihrke PJ, Walder EJ, and
Affolter VK, 2nd ed., pp. 199–399. Blackwell Science,
Ames, IA, 2005
5 Lothrop CD: Thyrotropin stimulation test for
evaluation of thyroid function in psittacine birds.
J Am Vet Med Assoc 186:47–48, 1985
Vet Pathol 45:3, 2008
6 Lucas AM, Stettenheim PR: Avian anatomy. Integument. Agricultural handbook 362, pp. 485–635.
US Department of Agriculture, Washington, DC,
1972
7 Nett CS, Hosgood G, Heatley JJ, Foil CS, Tully TN:
Evaluation of intravenous flourescein in intradermal
allergy testing in psittacines. Vet Dermatol
14:323–332, 2003
8 Oglesbee BL: Hypothyroidism in a scarlet macaw.
J Am Vet Med Assoc 201:1599–1601, 1992
9 Parmentier HK, De Vries Reilingh G, Nieuwland
MGB: Kinetic and immunohistochemical characteristics of mitogen-induced cutaneous hypersensitivity
in chickens selected for antibody responsiveness. Vet
Immunol Immunopathol 66:367–376, 2003
10 Rosenthal KL, Morris DO, Maudlin EA, Ivey ES,
Peikes H: Cytologic, histologic and microbiologic
characterization of the feather pulp and follicles of
feather-picking psittacines birds: a preliminary
study. J Avian Med Surg 18:137–143, 2004
11 Schmidt R: Use of biopsies in the differential
diagnosis of feather picking and avian skin disease,
Proc Assoc Avian Vet, Nashville, TN, pp. 113–118,
1993.
12 Schmidt RE, Lightfoot TL: 2006. Integument. In:
Clinical Avian Medicine, ed. Harrison GJ and
Lightfoot TL, vol. 1, pp. 395–410. Spix Publishing,
Palm Beach, FL, 2006
13 Van Belle G, Millard SP: STRUTS: Statistical Rules
of ThumbE, pp. 3–14. Departments of Environmental Health and Biostatistics, University of
Washington, Seattle, WA, 1998
Request reprints from Dr. Michael M. Garner, Northwest ZooPath, 654 West Main, Monroe, WA 98296 (USA).
E-mail: [email protected].